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Plant and Cell Physiology Advance Access originally published online on February 19, 2008
Plant and Cell Physiology 2008 49(4):549-556; doi:10.1093/pcp/pcn028
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© The Author 2008. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists. All rights reserved. For permissions, please email: journals.permissions@oxfordjournals.org

Nascent Peptide-Mediated Translation Elongation Arrest of Arabidopsis thaliana CGS1 mRNA Occurs Autonomously

Hitoshi Onouchi1, Yuhi Haraguchi1, Mari Nakamoto1,3, Daisuke Kawasaki2, Yoko Nagami-Yamashita1,4, Katsunori Murota2, Azusa Kezuka-Hosomi1,5, Yukako Chiba1,6 and Satoshi Naito1,2,*

1Division of Applied Bioscience, Graduate School of Agriculture, Hokkaido University, Sapporo, 060-8589 Japan
2Division of Life Science, Graduate School of Life Science, Hokkaido University, Sapporo, 060-8589 Japan

*Corresponding author: E-mail, naito{at}abs.agr.hokudai.ac.jp; Fax, +81-11-706-4932.


  Abstract

The Arabidopsis thaliana CGS1 gene encodes cystathionine {gamma}-synthase, the first committed enzyme of methionine biosynthesis in higher plants. Expression of CGS1 is feedback-regulated at the step of mRNA degradation in response to S-adenosyl-L-methionine (AdoMet). A short stretch of amino acid sequence, termed the MTO1 region, encoded within the first exon of CGS1 itself acts in cis in the regulation. In vitro analyses using wheat germ extract (WGE) revealed that AdoMet induces temporal translation arrest of CGS1 mRNA prior to mRNA degradation. This translational pausing occurs immediately downstream of the MTO1 region and is mediated by the nascent MTO1 peptide. In order to elucidate further the nature of this unique regulatory mechanism, we have examined whether a non-plant system also contains the post-transcriptional regulation activity. Despite the fact that mammals do not carry cystathionine {gamma}-synthase, AdoMet was able to induce the MTO1 sequence-dependent translation elongation arrest in rabbit reticulocyte lysate (RRL) in a similar manner to that observed in WGE. This result suggests that MTO1 peptide-mediated translation arrest does not require a plant-specific factor and rather most probably occurs via a direct interaction between the nascent MTO1 peptide and the ribosome that has translated it. In contrast, decay intermediates of CGS1 mRNA normally observed upon induction of CGS1 mRNA decay in plant systems were not detected in RRL, raising the possibility that CGS1 mRNA degradation involves a plant-specific mechanism.

Keywords: S-Adenosyl-L-methionine - Arabidopsis thaliana - In vitro translation - Methionine biosynthesis - mRNA stability - Translation elongation arrest

Abbreviations: AdoMet, S-adenosyl-L-methionine; CGS, cystathionine {gamma}-synthase; CTAB, cetyltrimethylammonium bromide; GST, glutathione S-transferase; LUC, firefly luciferase; ORF, open reading frame; RLUC, sea pansy luciferase; RRL, rabbit reticulocyte lysate; uORF, upstream ORF; WGE, wheat germ extract.

3Present address: Life Science Group, Olympus Corp., Hachioji, 192-8512 Japan.

4Present address: Plant Genetic Resources Division, Hokkaido Central Agricultural Experiment Station, Takikawa, 073-0013 Japan.

5Present address: Tobacco Science Research Center, Japan Tobacco Inc., Yokohama, 227-8512 Japan.

6Present address: Research Institute for Bioresources, Okayama University, Kurashiki, 710-0046 Japan.

(Received January 21, 2007; Accepted February 14, 2008)
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